{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T00:52:47Z","timestamp":1790815967209,"version":"4.1.0"},"reference-count":24,"publisher":"National Academy of Sciences","issue":"2","license":[{"start":{"date-parts":[[2018,6,28]],"date-time":"2018-06-28T00:00:00Z","timestamp":1530144000000},"content-version":"vor","delay-in-days":182,"URL":"http:\/\/www.pnas.org\/site\/aboutpnas\/licenses.xhtml"}],"funder":[{"DOI":"10.13039\/501100003246","name":"Nederlandse Organisatie voor Wetenschappelijk Onderzoek","doi-asserted-by":"publisher","award":["NWO-VICI-91812628"],"award-info":[{"award-number":["NWO-VICI-91812628"]}],"id":[{"id":"10.13039\/501100003246","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["SFB685"],"award-info":[{"award-number":["SFB685"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100010269","name":"Wellcome","doi-asserted-by":"publisher","award":["102572\/B\/13\/Z"],"award-info":[{"award-number":["102572\/B\/13\/Z"]}],"id":[{"id":"10.13039\/100010269","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100010269","name":"Wellcome","doi-asserted-by":"publisher","award":["108466\/Z\/15\/Z"],"award-info":[{"award-number":["108466\/Z\/15\/Z"]}],"id":[{"id":"10.13039\/100010269","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.pnas.org"],"crossmark-restriction":true},"short-container-title":["Proc. Natl. Acad. Sci. U.S.A."],"published-print":{"date-parts":[[2018,1,9]]},"abstract":"<jats:title>Significance<\/jats:title>\n                  <jats:p>Acute hemorrhagic conjunctivitis (AHC) is a painful and highly contagious infection of the eye, with reported incidence rates of up to 48%. No drugs or vaccines are available for treatment or prevention of AHC. Coxsackievirus A24 variant (CV-A24v) is the main etiological agent of AHC, being responsible for &gt;10 million AHC cases worldwide during the last decades. We have identified the CV-A24v protein receptor and determined the high-resolution structure of the virus\u2013receptor complex. Furthermore, we found that an adaptation which enhances binding to the receptor sialic acid may have contributed to the pathogenicity and pandemic nature of CV-A24v. These findings highlight the importance of sialic acid for viruses with ocular tropism, such as influenza A virus and several adenoviruses.<\/jats:p>","DOI":"10.1073\/pnas.1713284115","type":"journal-article","created":{"date-parts":[[2017,12,28]],"date-time":"2017-12-28T15:30:38Z","timestamp":1514475038000},"page":"397-402","update-policy":"https:\/\/doi.org\/10.1073\/pnas.cm10313","source":"Crossref","is-referenced-by-count":58,"title":["Role of enhanced receptor engagement in the evolution of a pandemic acute hemorrhagic conjunctivitis virus"],"prefix":"10.1073","volume":"115","author":[{"given":"Jim","family":"Baggen","sequence":"first","affiliation":[{"name":"Virology Division, Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, 3584CL Utrecht, The Netherlands;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3834-5808","authenticated-orcid":false,"given":"Daniel L.","family":"Hurdiss","sequence":"additional","affiliation":[{"name":"Astbury Centre for Structural Molecular Biology, Faculty of Biological Sciences, University of Leeds, Leeds LS2 9JT, United Kingdom;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Georg","family":"Zocher","sequence":"additional","affiliation":[{"name":"Interfaculty Institute of Biochemistry, University of T\u00fcbingen, 72076 T\u00fcbingen, Germany;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nitesh","family":"Mistry","sequence":"additional","affiliation":[{"name":"Division of Virology, Department of Clinical Microbiology, Ume\u00e5 University, 90187 Ume\u00e5, Sweden;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Richard W.","family":"Roberts","sequence":"additional","affiliation":[{"name":"Virology Division, Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, 3584CL Utrecht, The Netherlands;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jasper J.","family":"Slager","sequence":"additional","affiliation":[{"name":"Virology Division, Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, 3584CL Utrecht, The Netherlands;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hongbo","family":"Guo","sequence":"additional","affiliation":[{"name":"Virology Division, Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, 3584CL Utrecht, The Netherlands;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Arno L. W.","family":"van Vliet","sequence":"additional","affiliation":[{"name":"Virology Division, Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, 3584CL Utrecht, The Netherlands;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maryam","family":"Wahedi","sequence":"additional","affiliation":[{"name":"Virology Division, Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, 3584CL Utrecht, The Netherlands;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kimberley","family":"Benschop","sequence":"additional","affiliation":[{"name":"Centre for Infectious Disease Control, National Institute for Public Health and the Environment, 3720BA Bilthoven, The Netherlands;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Erwin","family":"Duizer","sequence":"additional","affiliation":[{"name":"Centre for Infectious Disease Control, National Institute for Public Health and the Environment, 3720BA Bilthoven, The Netherlands;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cornelis A. M.","family":"de Haan","sequence":"additional","affiliation":[{"name":"Virology Division, Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, 3584CL Utrecht, The Netherlands;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Erik","family":"de Vries","sequence":"additional","affiliation":[{"name":"Virology Division, Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, 3584CL Utrecht, The Netherlands;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jos\u00e9 M.","family":"Casasnovas","sequence":"additional","affiliation":[{"name":"Department of Macromolecular Structures, Centro Nacional de Biotecnolog\u00eda, Campus Universidad Aut\u00f3noma de Madrid, 28049 Madrid, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Raoul J.","family":"de Groot","sequence":"additional","affiliation":[{"name":"Virology Division, Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, 3584CL Utrecht, The Netherlands;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7069-6678","authenticated-orcid":false,"given":"Niklas","family":"Arnberg","sequence":"additional","affiliation":[{"name":"Division of Virology, Department of Clinical Microbiology, Ume\u00e5 University, 90187 Ume\u00e5, Sweden;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Thilo","family":"Stehle","sequence":"additional","affiliation":[{"name":"Interfaculty Institute of Biochemistry, University of T\u00fcbingen, 72076 T\u00fcbingen, Germany;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3640-5275","authenticated-orcid":false,"given":"Neil A.","family":"Ranson","sequence":"additional","affiliation":[{"name":"Astbury Centre for Structural Molecular Biology, Faculty of Biological Sciences, University of Leeds, Leeds LS2 9JT, United Kingdom;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hendrik Jan","family":"Thibaut","sequence":"additional","affiliation":[{"name":"Virology Division, Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, 3584CL Utrecht, The Netherlands;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Frank J. M.","family":"van Kuppeveld","sequence":"additional","affiliation":[{"name":"Virology Division, Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, 3584CL Utrecht, The Netherlands;"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"341","published-online":{"date-parts":[[2017,12,28]]},"reference":[{"key":"e_1_3_4_1_2","first-page":"511","article-title":"An outbreak of acute haemorrhagic conjunctivitis in Melaka, Malaysia","volume":"44","author":"Ghazali O","year":"2003","unstructured":"O Ghazali, , An outbreak of acute haemorrhagic conjunctivitis in Melaka, Malaysia. Singapore Med J 44, 511\u2013516 (2003).","journal-title":"Singapore Med J"},{"key":"e_1_3_4_2_2","first-page":"904","article-title":"Viral investigation of acute hemorrhagic conjunctivitis outbreak (2003) in Nepal using molecular methods","volume":"37","author":"Kurokawa M","year":"2006","unstructured":"M Kurokawa, SK Rai, K Ono, R Gurung, S Ruit, Viral investigation of acute hemorrhagic conjunctivitis outbreak (2003) in Nepal using molecular methods. Southeast Asian J Trop Med Public Health 37, 904\u2013910 (2006).","journal-title":"Southeast Asian J Trop Med Public Health"},{"key":"e_1_3_4_3_2","doi-asserted-by":"crossref","first-page":"1010","DOI":"10.3201\/eid0908.030190","article-title":"Acute hemorrhagic conjunctivitis caused by coxsackievirus A24 variant, South Korea, 2002","volume":"9","author":"Oh MD","year":"2003","unstructured":"MD Oh, , Acute hemorrhagic conjunctivitis caused by coxsackievirus A24 variant, South Korea, 2002. Emerg Infect Dis 9, 1010\u20131012 (2003).","journal-title":"Emerg Infect Dis"},{"key":"e_1_3_4_4_2","first-page":"421","article-title":"Studies in poliomyelitis; the isolation of a coxsackie-like virus from the faeces of apparently healthy bantu infants","volume":"25","author":"Measroch V","year":"1951","unstructured":"V Measroch, J Gear, GI Faerber, Studies in poliomyelitis; the isolation of a coxsackie-like virus from the faeces of apparently healthy bantu infants. S Afr Med J 25, 421\u2013424 (1951).","journal-title":"S Afr Med J"},{"key":"e_1_3_4_5_2","doi-asserted-by":"crossref","first-page":"1191","DOI":"10.1016\/S0140-6736(72)90921-X","article-title":"Pandemic of new type of conjunctivitis","volume":"1","author":"Kono R","year":"1972","unstructured":"R Kono, A Sasagawa, K Ishii, S Sugiura, M Ochi, Pandemic of new type of conjunctivitis. Lancet 1, 1191\u20131194 (1972).","journal-title":"Lancet"},{"key":"e_1_3_4_6_2","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1159\/000149850","article-title":"Enterovirus etiology of the 1970 Singapore epidemic of acute conjunctivitis","volume":"4","author":"Mirkovic RR","year":"1974","unstructured":"RR Mirkovic, NJ Schmidt, M Yin-Murphy, JL Melnick, Enterovirus etiology of the 1970 Singapore epidemic of acute conjunctivitis. Intervirology 4, 119\u2013127 (1974).","journal-title":"Intervirology"},{"key":"e_1_3_4_7_2","doi-asserted-by":"crossref","first-page":"159","DOI":"10.7883\/yoken1952.41.159","article-title":"The first epidemic of acute hemorrhagic conjunctivitis due to a coxsackievirus A24 variant in Okinawa, Japan, in 1985-1986","volume":"41","author":"Miyamura K","year":"1988","unstructured":"K Miyamura, , The first epidemic of acute hemorrhagic conjunctivitis due to a coxsackievirus A24 variant in Okinawa, Japan, in 1985-1986. Jpn J Med Sci Biol 41, 159\u2013174 (1988).","journal-title":"Jpn J Med Sci Biol"},{"key":"e_1_3_4_8_2","doi-asserted-by":"crossref","first-page":"748","DOI":"10.1016\/0042-6822(92)90477-7","article-title":"Phylogenetic analysis of a coxsackievirus A24 variant: The most recent worldwide pandemic was caused by progenies of a virus prevalent around 1981","volume":"187","author":"Ishiko H","year":"1992","unstructured":"H Ishiko, , Phylogenetic analysis of a coxsackievirus A24 variant: The most recent worldwide pandemic was caused by progenies of a virus prevalent around 1981. Virology 187, 748\u2013759 (1992).","journal-title":"Virology"},{"key":"e_1_3_4_9_2","doi-asserted-by":"crossref","first-page":"212","DOI":"10.1016\/j.medmal.2009.09.006","article-title":"Les Enterovirus responsables de conjonctivite aigu\u00eb h\u00e9morragique","volume":"40","author":"L\u00e9v\u00eaque N","year":"2010","unstructured":"N L\u00e9v\u00eaque, P Huguet, H Norder, J-J Chomel, Les Enterovirus responsables de conjonctivite aigu\u00eb h\u00e9morragique. Med Mal Infect 40, 212\u2013218 (2010).","journal-title":"Med Mal Infect"},{"key":"e_1_3_4_10_2","doi-asserted-by":"crossref","first-page":"324","DOI":"10.1016\/S0966-842X(02)02383-1","article-title":"Picornavirus-receptor interactions","volume":"10","author":"Rossmann MG","year":"2002","unstructured":"MG Rossmann, Y He, RJ Kuhn, Picornavirus-receptor interactions. Trends Microbiol 10, 324\u2013331 (2002).","journal-title":"Trends Microbiol"},{"key":"e_1_3_4_11_2","doi-asserted-by":"crossref","first-page":"3061","DOI":"10.1128\/JVI.02470-07","article-title":"Sialic acid is a cellular receptor for coxsackievirus A24 variant, an emerging virus with pandemic potential","volume":"82","author":"Nilsson EC","year":"2008","unstructured":"EC Nilsson, F Jamshidi, SMC Johansson, MS Oberste, N Arnberg, Sialic acid is a cellular receptor for coxsackievirus A24 variant, an emerging virus with pandemic potential. J Virol 82, 3061\u20133068 (2008).","journal-title":"J Virol"},{"key":"e_1_3_4_12_2","doi-asserted-by":"crossref","first-page":"e1004401","DOI":"10.1371\/journal.ppat.1004401","article-title":"A sialic acid binding site in a human picornavirus","volume":"10","author":"Zocher G","year":"2014","unstructured":"G Zocher, , A sialic acid binding site in a human picornavirus. PLoS Pathog 10, e1004401 (2014).","journal-title":"PLoS Pathog"},{"key":"e_1_3_4_13_2","doi-asserted-by":"crossref","first-page":"1399","DOI":"10.1073\/pnas.1524498113","article-title":"Enterovirus D68 receptor requirements unveiled by haploid genetics","volume":"113","author":"Baggen J","year":"2016","unstructured":"J Baggen, , Enterovirus D68 receptor requirements unveiled by haploid genetics. Proc Natl Acad Sci USA 113, 1399\u20131404, and correction (2016) 113:E1588 (2016).","journal-title":"Proc Natl Acad Sci USA"},{"key":"e_1_3_4_14_2","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1007\/BF00202069","article-title":"Intercellular adhesion molecule-1","volume":"74","author":"van de Stolpe A","year":"1996","unstructured":"A van de Stolpe, PT van der Saag, Intercellular adhesion molecule-1. J Mol Med (Berl) 74, 13\u201333 (1996).","journal-title":"J Mol Med (Berl)"},{"key":"e_1_3_4_15_2","doi-asserted-by":"crossref","first-page":"785","DOI":"10.1128\/jvi.71.1.785-789.1997","article-title":"Mouse cells expressing human intercellular adhesion molecule-1 are susceptible to infection by coxsackievirus A21","volume":"71","author":"Shafren DR","year":"1997","unstructured":"DR Shafren, DJ Dorahy, SJ Greive, GF Burns, RD Barry, Mouse cells expressing human intercellular adhesion molecule-1 are susceptible to infection by coxsackievirus A21. J Virol 71, 785\u2013789 (1997).","journal-title":"J Virol"},{"key":"e_1_3_4_16_2","doi-asserted-by":"crossref","first-page":"839","DOI":"10.1016\/0092-8674(89)90688-0","article-title":"The major human rhinovirus receptor is ICAM-1","volume":"56","author":"Greve JM","year":"1989","unstructured":"JM Greve, , The major human rhinovirus receptor is ICAM-1. Cell 56, 839\u2013847 (1989).","journal-title":"Cell"},{"key":"e_1_3_4_17_2","doi-asserted-by":"crossref","first-page":"1320","DOI":"10.1126\/science.275.5304.1320","article-title":"Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5","volume":"275","author":"Bergelson JM","year":"1997","unstructured":"JM Bergelson, , Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 275, 1320\u20131323 (1997).","journal-title":"Science"},{"key":"e_1_3_4_18_2","doi-asserted-by":"crossref","first-page":"1019","DOI":"10.1016\/j.str.2005.04.011","article-title":"The crystal structure of coxsackievirus A21 and its interaction with ICAM-1","volume":"13","author":"Xiao C","year":"2005","unstructured":"C Xiao, , The crystal structure of coxsackievirus A21 and its interaction with ICAM-1. Structure 13, 1019\u20131033 (2005).","journal-title":"Structure"},{"key":"e_1_3_4_19_2","doi-asserted-by":"crossref","first-page":"11808","DOI":"10.1073\/pnas.94.22.11808","article-title":"Structural evidence for a second sialic acid binding site in avian influenza virus neuraminidases","volume":"94","author":"Varghese JN","year":"1997","unstructured":"JN Varghese, , Structural evidence for a second sialic acid binding site in avian influenza virus neuraminidases. Proc Natl Acad Sci USA 94, 11808\u201311812 (1997).","journal-title":"Proc Natl Acad Sci USA"},{"key":"e_1_3_4_20_2","first-page":"E3111","article-title":"Coronavirus receptor switch explained from the stereochemistry of protein-carbohydrate interactions and a single mutation","volume":"113","author":"Bakkers MJG","year":"2016","unstructured":"MJG Bakkers, , Coronavirus receptor switch explained from the stereochemistry of protein-carbohydrate interactions and a single mutation. Proc Natl Acad Sci USA 113, E3111\u2013E3119 (2016).","journal-title":"Proc Natl Acad Sci USA"},{"key":"e_1_3_4_21_2","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1128\/JVI.74.1.42-48.2000","article-title":"Adenovirus type 37 uses sialic acid as a cellular receptor","volume":"74","author":"Arnberg N","year":"2000","unstructured":"N Arnberg, K Edlund, AH Kidd, G Wadell, Adenovirus type 37 uses sialic acid as a cellular receptor. J Virol 74, 42\u201348 (2000).","journal-title":"J Virol"},{"key":"e_1_3_4_22_2","doi-asserted-by":"crossref","first-page":"11265","DOI":"10.1128\/JVI.76.22.11265-11272.2002","article-title":"Sialic acid functions in enterovirus 70 binding and infection","volume":"76","author":"Alexander DA","year":"2002","unstructured":"DA Alexander, K Dimock, Sialic acid functions in enterovirus 70 binding and infection. J Virol 76, 11265\u201311272 (2002).","journal-title":"J Virol"},{"key":"e_1_3_4_23_2","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1128\/MMBR.00058-12","article-title":"Ocular tropism of respiratory viruses","volume":"77","author":"Belser JA","year":"2013","unstructured":"JA Belser, PA Rota, TM Tumpey, Ocular tropism of respiratory viruses. Microbiol Mol Biol Rev 77, 144\u2013156 (2013).","journal-title":"Microbiol Mol Biol Rev"},{"key":"e_1_3_4_24_2","doi-asserted-by":"crossref","first-page":"e93737","DOI":"10.1371\/journal.pone.0093737","article-title":"The evolution of Vp1 gene in enterovirus C species sub-group that contains types CVA-21, CVA-24, EV-C95, EV-C96 and EV-C99","volume":"9","author":"Smura T","year":"2014","unstructured":"T Smura, , The evolution of Vp1 gene in enterovirus C species sub-group that contains types CVA-21, CVA-24, EV-C95, EV-C96 and EV-C99. PLoS One 9, e93737 (2014).","journal-title":"PLoS One"}],"container-title":["Proceedings of the National Academy of Sciences"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/www.pnas.org\/syndication\/doi\/10.1073\/pnas.1713284115","content-type":"unspecified","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/pnas.org\/doi\/pdf\/10.1073\/pnas.1713284115","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,6,7]],"date-time":"2022-06-07T13:59:43Z","timestamp":1654610383000},"score":1,"resource":{"primary":{"URL":"https:\/\/pnas.org\/doi\/full\/10.1073\/pnas.1713284115"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,12,28]]},"references-count":24,"journal-issue":{"issue":"2","published-print":{"date-parts":[[2018,1,9]]}},"alternative-id":["10.1073\/pnas.1713284115"],"URL":"https:\/\/doi.org\/10.1073\/pnas.1713284115","relation":{},"ISSN":["0027-8424","1091-6490"],"issn-type":[{"value":"0027-8424","type":"print"},{"value":"1091-6490","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,12,28]]},"assertion":[{"value":"2017-12-28","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}